RESEARCH Lack of Airborne Transmission during Outbreak of Pandemic (H1N1) 2009 among Tour Group Members, China, June 2009 Ke Han,1 Xiaoping Zhu,1 Fan He,1 Lunguang Liu, Lijie Zhang, Huilai Ma, Xinyu Tang, Ting Huang, Guang Zeng, and Bao-Ping Zhu During June 2–8, 2009, an outbreak of influenza A pan- start of the 2009 influenza pandemic (4). Investigations of demic (H1N1) 2009 occurred among 31 members of a tour transmission chains early in the pandemic will add to our group in China. To identify the mode of transmission and risk understanding of the special characteristics of this new vi- factors, we conducted a retrospective cohort investigation. rus, including whether its mode of transmission differs from The index case-patient was a female tourist from the United that of seasonal influenza viruses. This information will be States. Secondary cases developed in 9 (30%) tour group useful for effective control of the spread of this virus. members who had talked with the index case-patient and in 1 airline passenger (not a tour group member) who had sat In the People’s Republic of China, the early response within 2 rows of her. None of the 14 tour group members strategy has been containment, which includes temperature who had not talked with the index case-patient became ill. screening and administration of health questionnaires at This outbreak was apparently caused by droplet transmis- international ports of entry, isolation of infected travelers, sion during coughing or talking. That airborne transmission and quarantine of close contacts of infected persons. Dur- was not a factor is supported by lack of secondary cases ing June 2–8, 2009, an outbreak of pandemic (H1N1) 2009 among fellow bus and air travelers. Our findings highlight occurred among members of a tour group. We investigated the need to prevent transmission by droplets and fomites this outbreak to identify the source of infection, mode of during a pandemic. transmission, and risk factors for infection. ince the emergence of a novel influenza A (H1N1) vi- Methods Srus (later called influenza A pandemic [H1N1] 2009 The index case-patient was a 40-year-old female US virus) in early 2009 in Mexico (1,2), the virus has spread to citizen who had traveled from the United States to Jiu- 156 countries, territories, and areas; as of July 27, 2009, a zhaigou, a popular tourist spot in southwestern China; she total of 134,503 laboratory-confirmed cases and 816 deaths stopped to change planes in Hong Kong and Chengdu. She had been reported (3). On June 11, 2009, the World Health noticed her first symptom, chills, on June 2, immediately Organization declared that the world was experiencing the before arriving in Chengdu, ≈23 hours after departure from the United States. After learning that she had traveled on 3 Author affiliations: Chinese Center for Disease Control and Preven- flights and had toured with a group, we obtained the mani- tion, Beijing, People’s Republic of China (K. Han, F. He, L. Zhang, fests of all flights that she had traveled on and asked all pas- H. Ma, G. Zeng, B.-P. Zhu); Guangdong Center for Disease Control sengers of the 3 flights and all members of the tour group and Prevention, Guangzhou, People’s Republic of China (K. Han); by telephone or in-person interview whether they had had Zhejiang Center for Disease Control and Prevention, Hangzhou, any symptoms from May 27 through June 12, 2009. We People’s Republic of China (F. He); and Sichuan Center for Dis- also obtained detailed information on the activities of the ease Control and Prevention, Sichuan, People’s Republic of China tour group during the 3-day tour. Health authorities placed (X. Zhu, L. Liu, X. Tang, T. Huang) members of the tour group under medical observation and DOI: 10.3201/eid1510.091013 1These authors contributed equally to this article. 1578 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 10, October 2009 Pandemic (H1N1) 2009, Tour Group, China isolated those who had clinical signs or symptoms or posi- 6 tive throat swab culture results. Laboratory technicians 5 at the Sichuan Province Center for Disease Control and 4 Prevention collected throat swabs every 24 hours from all s case 3 members of the tour group and from symptomatic persons No. 2 who had shared any of the 3 flights with the index case-pa- tient. Real-time reverse transcription–PCR (RT-PCR) was 1 0 performed to detect nucleic acids specific for the influenza AMPMAMPMAMPMAMPMAMPMAMPMAMPM A pandemic (H1N1) 2009 virus by using the primers sup- 2 3 4 5 6 7 8 plied by the World Health Organization. Day, June 2009 Figure 1. Time of disease onset for persons infected with influenza We defined a suspected case as onset of> 1 of 5 symp- toms—fever (>38°C), cough, sore throat, chills, or head- A pandemic (H1N1) 2009 virus, Sichuan Province, China, June ache—in a passenger of flight CZ6659 (June 3, Chengdu 2009. to Jiuzhaigou) or flight CZ6660 (June 5, Jiuzhaigou to Chengdu) or in a member of the tour group. A confirmed flight CZ6660 (Boeing 757), which departed Jiuzhaigou at case was a suspected case for which real-time RT-PCR 1:30 PM and arrived in Chengdu at 2:15 PM , along with 87 provided laboratory confirmation of the influenza A pan- other passengers (Figure 2). demic (H1N1) 2009 virus infection. A secondary case was All airplanes boarded by the index case-patient had a confirmed case for which the patient’s signs or symptoms high-efficiency particulate air filters. Less than half of the began after 9:00 PM on June 3, i.e., at least 24 hours after the air in the passenger cabins was recirculated; the rest was onset of the primary (index) case. from outside. Air in the passenger cabins of the airplanes To identify the mode of transmission and risk factors was recirculated approximately every 3 minutes. The air for infection, we conducted a retrospective cohort investi- conditioning system in the tour bus mixed ≈70% recircu- gation. We interviewed all members of the tour group by lated inside air with ≈30% outside air, filtered it, and deliv- telephone or in-person interview to ascertain details of their ered it into the bus through air outlets above the passenger contact history with the index case-patient. seats. A vent at the back of the bus continually exhausted air from inside the bus. Results The diagnosis of influenza A pandemic (H1N1) 2009 During this outbreak, we identified a total of 11 con- virus infection was made for the index case-patient after she firmed cases of influenza A pandemic (H1N1) 2009 infec- returned to Chengdu on June 5. Subsequently, members of tion (Figure 1). Average patient age was 36 (range 18–59) the tour group were placed under involuntary medical ob- years; 2 patients were men and 9 were women. Signs and servation. No influenza-like illness developed in any of the symptoms were cough (73%), fever (64%), sore throat 91 passengers of flight CA428 (Hong Kong to Chengdu) (64%), headache (27%), chills (27%), runny nose (18%), or in any of the 87 passengers on flight CZ6659 (Chengdu and myalgia (18%). All 11 case-patients fully recovered; 3 to Jiuzhaigou) who were not members of the tour group. (including the index case-patient) recovered on June 13, 5 on June 15, 1 on June 17, and 2 on June 18. The mean dura- tion of illness was 11 (range 9–14) days. The index case-patient left New York City, United States, on flight CX841 at 12:00 AM (midnight) June 2 and arrived in Hong Kong at 2:00 PM on the same day. She transferred to flight CA428 (Boeing 757), which de- parted Hong Kong at 7:25 PM and arrived in Chengdu at 10:00 PM . On June 3, she and her family members joined the tour group at the Chengdu Airport and boarded flight CZ6659 (Boeing 757), which departed Chengdu at 12:25 PM and arrived at Jiuzhaigou (33°15′55′′N, 104°13′35′′E; average altitude 2,930 m) at 1:10 PM . The group picked up 7 additional members in Jiuzhaigou, where they traveled to various tourist attractions by bus and participated in group Figure 2. Timeline of exposures to the index case-patient during activities during the ensuing 3 days. On June 5, the original outbreak of influenza A pandemic (H1N1) 2009, Sichuan Province, 24 members of the tour group from Chengdu (without the 7 China, June 2009. Numbers in parentheses indicate number of members who had joined the group in Jiuzhaigou) boarded persons exposed. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 10, October 2009 1579 RESEARCH None of the passengers on either flight had donned a mask. same table, sitting within 2 rows on the same flight or bus However, excluding the index case-patient, 9 (30%) of the ride, and receiving chewing gum from her. Moreover, 3 of 30 members of the tour group became ill with secondary these 14 uninfected passengers had sat within 2 seats of the cases of disease. The secondary attack rate did not differ index case-patient during the bus rides but had never talked between the members of the tour group who flew from with her from close range. Chengdu to Jiuzhaigou and the members who joined the tour in Jiuzhaigou. Of the 87 passengers on the return flight Discussion (Jiuzhaigou to Chengdu) on June 5 who were not members Since its emergence, pandemic (H1N1) 2009 has of the tour group, 1 person became ill (Table 1).